The Relationship between Associative Learning, Transfer Generalization, and Homocysteine Levels in Mild Cognitive Impairment

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Moustafa, Ahmed A ^a   Hewedi, Doaa H ^b   Eissa, Abeer M ^b   Myers, Catherine E ^c,d   Sadek, Hisham A ^b  

^a WESTERN SYDNEY UNIVERSITY   (Australia)

^b AIN SHAMS UNIVERSITY   (Egypt)

^c RUTGERS UNIVERSITY   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMOCYSTEINE;

AGED; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE ASSOCIATION; FEMALE; HIPPOCAMPUS; HUMAN; LEARNING; MALE; MENTAL TASK; MILD COGNITIVE IMPAIRMENT; PATIENT CODING; SCORING SYSTEM; TRANSFER GENERALIZATION;

AGED; ASSOCIATION LEARNING; CASE-CONTROL STUDIES; FEMALE; GENERALIZATION (PSYCHOLOGY); HOMOCYSTEINE; HUMANS; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; TRANSFER (PSYCHOLOGY);

EID: 84866980554     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046496     Document Type: Article

References (101)

1. Ayesa-Arriola R, Perez-Iglesias R, Rodriguez-Sanchez JM, Mata I, Gomez-Ruiz E, et al. (2012) Homocysteine and cognition in first-episode psychosis patients. Eur Arch Psychiatry Clin Neurosci.
2. Sachdev PS, (2005) Homocysteine and brain atrophy. Prog Neuropsychopharmacol Biol Psychiatry 29: 1152-1161.
3. Faux NG, Ellis KA, Porter L, Fowler CJ, Laws SM, et al. (2011) Homocysteine, vitamin B12, and folic acid levels in Alzheimer's disease, mild cognitive impairment, and healthy elderly: baseline characteristics in subjects of the Australian Imaging Biomarker Lifestyle study. J Alzheimers Dis 27: 909-922.
4. Ho RC, Cheung MW, Fu E, Win HH, Zaw MH, et al. (2011) Is high homocysteine level a risk factor for cognitive decline in elderly? A systematic review, meta-analysis, and meta-regression. Am J Geriatr Psychiatry 19: 607-617.
5. Weiner MF, de la Plata CM, Fields BA, Womack KB, Rosenberg RN, et al. (2009) Brain MRI, apoliprotein E genotype, and plasma homocysteine in American Indian Alzheimer disease patients and Indian controls. Curr Alzheimer Res 6: 52-58.
6. Zhuo JM, Wang H, Pratico D, (2011) Is hyperhomocysteinemia an Alzheimer's disease (AD) risk factor, an AD marker, or neither? Trends Pharmacol Sci 32: 562-571.
7. Hooshmand B, Solomon A, Kareholt I, Leiviska J, Rusanen M, et al. (2010) Homocysteine and holotranscobalamin and the risk of Alzheimer disease: a longitudinal study. Neurology 75: 1408-1414.
8. Kim J, Park MH, Kim E, Han C, Jo SA, et al. (2007) Plasma homocysteine is associated with the risk of mild cognitive impairment in an elderly Korean population. J Nutr 137: 2093-2097.
9. Ganguly PK, Maddaford TG, Edel AL, O K, Smeda JS, et al. (2008) Increased homocysteine-induced release of excitatory amino acids in the striatum of spontaneously hypertensive stroke-prone rats. Brain Res 1226: 192-198.
10. Zoccolella S, Martino D, Defazio G, Lamberti P, Livrea P, (2006) Hyperhomocysteinemia in movement disorders: Current evidence and hypotheses. Curr Vasc Pharmacol 4: 237-243.
11. Oulhaj A, Refsum H, Beaumont H, Williams J, King E, et al. (2010) Homocysteine as a predictor of cognitive decline in Alzheimer's disease. Int J Geriatr Psychiatry 25: 82-90.
12. McCaddon A, Hudson P, Davies G, Hughes A, Williams JH, et al. (2001) Homocysteine and cognitive decline in healthy elderly. Dement Geriatr Cogn Disord 12: 309-313.
13. Annerbo S, Wahlund LO, Lokk J, (2005) The relation between homocysteine levels and development of Alzheimer's disease in mild cognitive impairment patients. Dement Geriatr Cogn Disord 20: 209-214.
14. Pirchl M, Ullrich C, Humpel C, (2010) Differential effects of short- and long-term hyperhomocysteinaemia on cholinergic neurons, spatial memory and microbleedings in vivo in rats. Eur J Neurosci 32: 1516-1527.
15. Oddo S, LaFerla FM, (2006) The role of nicotinic acetylcholine receptors in Alzheimer's disease. J Physiol Paris 99: 172-179.
16. Maelicke A, Albuquerque EX, (2000) Allosteric modulation of nicotinic acetylcholine receptors as a treatment strategy for Alzheimer's disease. Eur J Pharmacol 393: 165-170.
17. Sabri O, Kendziorra K, Wolf H, Gertz HJ, Brust P, (2008) Acetylcholine receptors in dementia and mild cognitive impairment. Eur J Nucl Med Mol Imaging 35 Suppl 1: S30-45.
18. Maelicke A, (2000) Allosteric modulation of nicotinic receptors as a treatment strategy for Alzheimer's disease. Dement Geriatr Cogn Disord 11 Suppl 1: 11-18.
19. Ikonomovic MD, Mufson EJ, Wuu J, Cochran EJ, Bennett DA, et al. (2003) Cholinergic plasticity in hippocampus of individuals with mild cognitive impairment: correlation with Alzheimer's neuropathology. J Alzheimers Dis 5: 39-48.
20. Smith AD, Smith SM, de Jager CA, Whitbread P, Johnston C, et al. (2010) Homocysteine-lowering by B vitamins slows the rate of accelerated brain atrophy in mild cognitive impairment: a randomized controlled trial. PLoS One 5: e12244.
21. Baydas G, Ozer M, Yasar A, Tuzcu M, Koz ST, (2005) Melatonin improves learning and memory performances impaired by hyperhomocysteinemia in rats. Brain Res 1046: 187-194.
22. Gao L, Zeng XN, Guo HM, Wu XM, Chen HJ, et al. (2011) Cognitive and neurochemical alterations in hyperhomocysteinemic rat. Neurol Sci 33: 39-43.
23. Logue SF, Paylor R, Wehner JM, (1997) Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behav Neurosci 111: 104-113.
24. Redish AD, Touretzky DS, (1998) The role of the hippocampus in solving the Morris water maze. Neural Comput 10: 73-111.
25. Nurk E, Refsum H, Tell GS, Engedal K, Vollset SE, et al. (2005) Plasma total homocysteine and memory in the elderly: the Hordaland Homocysteine Study. Ann Neurol 58: 847-857.
26. Hooshmand B, Solomon A, Kareholt I, Rusanen M, Hanninen T, et al. (2012) Associations between serum homocysteine, holotranscobalamin, folate and cognition in the elderly: a longitudinal study. J Intern Med 271: 204-212.
27. Dufouil C, Alperovitch A, Ducros V, Tzourio C, (2003) Homocysteine, white matter hyperintensities, and cognition in healthy elderly people. Ann Neurol 53: 214-221.
28. Teunissen CE, Blom AH, Van Boxtel MP, Bosma H, de Bruijn C, et al. (2003) Homocysteine: a marker for cognitive performance? A longitudinal follow-up study. J Nutr Health Aging 7: 153-159.
29. Prins ND, Den Heijer T, Hofman A, Koudstaal PJ, Jolles J, et al. (2002) Homocysteine and cognitive function in the elderly: the Rotterdam Scan Study. Neurology 59: 1375-1380.
30. Feng L, Ng TP, Chuah L, Niti M, Kua EH, (2006) Homocysteine, folate, and vitamin B-12 and cognitive performance in older Chinese adults: findings from the Singapore Longitudinal Ageing Study. Am J Clin Nutr 84: 1506-1512.
31. van den Kommer TN, Dik MG, Comijs HC, Jonker C, Deeg DJ, (2010) Homocysteine and inflammation: predictors of cognitive decline in older persons? Neurobiol Aging 31: 1700-1709.
32. Garcia A, Haron Y, Pulman K, Hua L, Freedman M, (2004) Increases in homocysteine are related to worsening of stroop scores in healthy elderly persons: a prospective follow-up study. J Gerontol A Biol Sci Med Sci 59: 1323-1327.
33. Narayan SK, Saxby BK, Firbank MJ, O'Brien JT, Harrington F, et al. (2011) Plasma homocysteine and cognitive decline in older hypertensive subjects. Int Psychogeriatr 23: 1607-1615.
34. Algaidi SA, Christie LA, Jenkinson AM, Whalley L, Riedel G, et al. (2006) Long-term homocysteine exposure induces alterations in spatial learning, hippocampal signalling and synaptic plasticity. Exp Neurol 197: 8-21.
35. Christie LA, Riedel G, Algaidi SA, Whalley LJ, Platt B, (2005) Enhanced hippocampal long-term potentiation in rats after chronic exposure to homocysteine. Neurosci Lett 373: 119-124.
36. Macpherson H, Ellis KA, Sali A, Pipingas A, (2012) Memory improvements in elderly women following 16 weeks treatment with a combined multivitamin, mineral and herbal supplement: A randomized controlled trial. Psychopharmacology (Berl) 220: 351-365.
37. Chen CS, Kuo YT, Tsai HY, Li CW, Lee CC, et al. (2011) Brain biochemical correlates of the plasma homocysteine level: a proton magnetic resonance spectroscopy study in the elderly subjects. Am J Geriatr Psychiatry 19: 618-626.
38. Matte C, Pereira LO, Dos Santos TM, Mackedanz V, Cunha AA, et al. (2009) Acute homocysteine administration impairs memory consolidation on inhibitory avoidance task and decreases hippocampal brain-derived neurotrophic factor immunocontent: prevention by folic acid treatment. Neuroscience 163: 1039-1045.
39. den Heijer T, Vermeer SE, Clarke R, Oudkerk M, Koudstaal PJ, et al. (2003) Homocysteine and brain atrophy on MRI of non-demented elderly. Brain 126: 170-175.
40. Genedani S, Agnati LF, Leo G, Buzzega D, Maccari F, et al. (2010) beta-Amyloid fibrillation and/or hyperhomocysteinemia modify striatal patterns of hyaluronic acid and dermatan sulfate: Possible role in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res 7: 150-157.
41. Rajagopalan P, Hua X, Toga AW, Jack CR Jr, Weiner MW, et al. (2011) Homocysteine effects on brain volumes mapped in 732 elderly individuals. Neuroreport 22: 391-395.
42. Gauthier S, Reisberg B, Zaudig M, Petersen RC, Ritchie K, et al. (2006) Mild cognitive impairment. Lancet 367: 1262-1270.
43. Flicker C, Ferris SH, Reisberg B, (1991) Mild cognitive impairment in the elderly: predictors of dementia. Neurology 41: 1006-1009.
44. Morris JC, Storandt M, Miller JP, McKeel DW, Price JL, et al. (2001) Mild cognitive impairment represents early-stage Alzheimer disease. Arch Neurol 58: 397-405.
45. Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, et al. (2001) Current concepts in mild cognitive impairment. Arch Neurol 58: 1985-1992.
46. Bowen J, Teri L, Kukull W, McCormick W, McCurry SM, et al. (1997) Progression to dementia in patients with isolated memory loss. Lancet 349: 763-765.
47. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, et al. (1999) Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56: 303-308.
48. Petersen RC, Stevens JC, Ganguli M, Tangalos EG, Cummings JL, et al. (2001) Practice parameter: early detection of dementia: mild cognitive impairment (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 56: 1133-1142.
49. Poldrack RA, Clark J, Pare-Blagoev EJ, Shohamy D, Creso Moyano J, et al. (2001) Interactive memory systems in the human brain. Nature 414: 546-550.
50. Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM, (1999) Building neural representations of habits. Science 286: 1745-1749.
51. Vandenberghe R, Dupont P, Bormans G, Mortelmans L, Orban GA, (1999) Brain activity underlying stereotyped and non-stereotyped retrieval of learned stimulus-response associations. Eur J Neurosci 11: 4037-4050.
52. Shohamy D, Myers CE, Geghman KD, Sage J, Gluck MA, (2006) L-dopa impairs learning, but spares generalization, in Parkinson's disease. Neuropsychologia 44: 774-784.
53. Gotham AM, Brown RG, Marsden CD, (1988) 'Frontal' cognitive function in patients with Parkinson's disease 'on' and 'off' levodopa. Brain 111 (Pt 2) (): 299-321.
54. Jahanshahi M, Wilkinson L, Gahir H, Dharminda A, Lagnado DA, (2009) Medication impairs probabilistic classification learning in Parkinson's disease. Neuropsychologia.
55. Seger CA, Spiering BJ, (2011) A critical review of habit learning and the Basal Ganglia. Front Syst Neurosci 5: 66.
56. Seger CA, Miller EK, (2010) Category learning in the brain. Annu Rev Neurosci 33: 203-219.
57. Eichenbaum H, Mathews P, Cohen NJ, (1989) Further studies of hippocampal representation during odor discrimination learning. Behav Neurosci 103: 1207-1216.
58. Young BJ, Fox GD, Eichenbaum H, (1994) Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task. J Neurosci 14: 6553-6563.
59. Myers, Gluck MA, (1994) Context, conditioning, and hippocampal rerepresentation in animal learning. Behav Neurosci 108: 835-847.
60. Wimmer GE, Daw ND, Shohamy D, (2012) Generalization of value in reinforcement learning by humans. Eur J Neurosci 35: 1092-1104.
61. Schacter DL, Rich SA, Stampp MS, (1985) Remediation of memory disorders: experimental evaluation of the spaced-retrieval technique. J Clin Exp Neuropsychol 7: 79-96.
62. Myers CE, Shohamy D, Gluck MA, Grossman S, Kluger A, et al. (2003) Dissociating hippocampal versus basal ganglia contributions to learning and transfer. J Cogn Neurosci 15: 185-193.
63. Myers CE, Hopkins RO, DeLuca J, Moore NB, Wolansky LJ, et al. (2008) Learning and generalization deficits in patients with memory impairments due to anterior communicating artery aneurysm rupture or hypoxic brain injury. Neuropsychology 22: 681-686.
64. Frank MJ, O'Reilly RC, Curran T, (2006) When memory fails, intuition reigns: midazolam enhances implicit inference in humans. Psychol Sci 17: 700-707.
65. Frank MJ, Rudy JW, O'Reilly RC, (2003) Transitivity, flexibility, conjunctive representations, and the hippocampus. II. A computational analysis. Hippocampus 13: 341-354.
66. Thompson R (1972) sensory preconditioning. In: Thompson RF, Voss JF, editors. Topics in learning and performance. New York,: Academic Press. pp. 105-129.
67. Bonardi C, Rey V, Richmond M, Hall G, (1993) Acquired equivalence of cues in pigeon autoshaping: Effects of training with common consequences and common antecedents. Animal Learning and Behavior 21: 369-376.
68. Johnson SC, Schmitz TW, Asthana S, Gluck MA, Myers C, (2007) Associative Learning Over Trials Activates the Hippocampus in Healthy Elderly but not Mild Cognitive Impairment. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn pp. 1-17.
69. Folstein MF, Folstein SE, McHugh PR, (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12: 189-198.
70. Morris JC, (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43: 2412-2414.
71. Morris JC, Price JL, (2001) Pathologic correlates of nondemented aging, mild cognitive impairment, and early-stage Alzheimer's disease. J Mol Neurosci 17: 101-118.
72. Perneczky R, Hartmann J, Grimmer T, Drzezga A, Kurz A, (2007) Cerebral metabolic correlates of the clinical dementia rating scale in mild cognitive impairment. J Geriatr Psychiatry Neurol 20: 84-88.
73. Reisberg B, Ferris SH, Kluger A, Franssen E, Wegiel J, et al. (2008) Mild cognitive impairment (MCI): a historical perspective. Int Psychogeriatr 20: 18-31.
74. Reisberg B, Ferris SH, de Leon MJ, Crook T, (1982) The Global Deterioration Scale for assessment of primary degenerative dementia. Am J Psychiatry 139: 1136-1139.
75. Kluger A, Ferris SH, Golomb J, Mittelman MS, Reisberg B, (1999) Neuropsychological prediction of decline to dementia in nondemented elderly. J Geriatr Psychiatry Neurol 12: 168-179.
76. Frantzen F, Faaren AL, Alfheim I, Nordhei AK, (1998) Enzyme conversion immunoassay for determining total homocysteine in plasma or serum. Clin Chem 44: 311-316.
77. Haan MN, Miller JW, Aiello AE, Whitmer RA, Jagust WJ, et al. (2007) Homocysteine, B vitamins, and the incidence of dementia and cognitive impairment: results from the Sacramento Area Latino Study on Aging. Am J Clin Nutr 85: 511-517.
78. Steinhauser M, Yeung N, (2010) Decision processes in human performance monitoring. J Neurosci 30: 15643-15653.
79. Krishna R, Moustafa AA, Eby LA, Skeen LC, Myers CE, (2012) Learning and generalization in healthy aging: implication for frontostriatal and hippocampal function. Cogn Behav Neurol 25: 7-15.
80. Stoub TR, deToledo-Morrell L, Stebbins GT, Leurgans S, Bennett DA, et al. (2006) Hippocampal disconnection contributes to memory dysfunction in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci U S A 103: 10041-10045.
81. Jack CR Jr, Petersen RC, Xu YC, O'Brien PC, Smith GE, et al. (1999) Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology 52: 1397-1403.
82. Apostolova LG, Dutton RA, Dinov ID, Hayashi KM, Toga AW, et al. (2006) Conversion of mild cognitive impairment to Alzheimer disease predicted by hippocampal atrophy maps. Arch Neurol 63: 693-699.
83. de Leon MJ, George AE, Stylopoulos LA, Smith G, Miller DC, (1989) Early marker for Alzheimer's disease: the atrophic hippocampus. Lancet 2: 672-673.
84. Killiany RJ, Moss MB, Albert MS, Sandor T, Tieman J, et al. (1993) Temporal lobe regions on magnetic resonance imaging identify patients with early Alzheimer's disease. Arch Neurol 50: 949-954.
85. Tamminen J, Davis MH, Merkx M, Rastle K, (2012) The role of memory consolidation in generalisation of new linguistic information. Cognition.
86. Kumaran D, McClelland JL, (2012) Generalization through the recurrent interaction of episodic memories: A model of the hippocampal system. Psychol Rev 119: 573-616.
87. Kumaran D, (2012) What representations and computations underpin the contribution of the hippocampus to generalization and inference? Front Hum Neurosci 6: 157.
88. Moustafa AA, Keri S, Herzallah MM, Myers CE, Gluck MA, (2010) A neural model of hippocampal-striatal interactions in associative learning and transfer generalization in various neurological and psychiatric patients. Brain Cogn 74: 132-144.
89. Pan X, Sakagami M, (2012) Category representation and generalization in the prefrontal cortex. Eur J Neurosci 35: 1083-1091.
90. Collins AG, Frank MJ, (2012) How much of reinforcement learning is working memory, not reinforcement learning? A behavioral, computational, and neurogenetic analysis. Eur J Neurosci 35: 1024-1035.
91. Jack CR Jr, Petersen RC, Xu Y, O'Brien PC, Smith GE, et al. (1998) Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease. Neurology 51: 993-999.
92. Jack CR Jr, Petersen RC, Xu Y, O'Brien PC, Smith GE, et al. (2000) Rates of hippocampal atrophy correlate with change in clinical status in aging and AD. Neurology 55: 484-489.
93. Grambaite R, Selnes P, Reinvang I, Aarsland D, Hessen E, et al. (2011) Executive dysfunction in mild cognitive impairment is associated with changes in frontal and cingulate white matter tracts. J Alzheimers Dis 27: 453-462.
94. Han Y, Lui S, Kuang W, Lang Q, Zou L, et al. (2012) Anatomical and functional deficits in patients with amnestic mild cognitive impairment. PLoS One 7: e28664.
95. Fouquet M, Desgranges B, Landeau B, Duchesnay E, Mezenge F, et al. (2009) Longitudinal brain metabolic changes from amnestic mild cognitive impairment to Alzheimer's disease. Brain 132: 2058-2067.
96. Eichenbaum H, Fagan A, Mathews P, Cohen NJ, (1988) Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. Behav Neurosci 102: 331-339.
97. Portet F, Ousset PJ, Visser PJ, Frisoni GB, Nobili F, et al. (2006) Mild cognitive impairment (MCI) in medical practice: a critical review of the concept and new diagnostic procedure. Report of the MCI Working Group of the European Consortium on Alzheimer's Disease. J Neurol Neurosurg Psychiatry 77: 714-718.
98. van Rossum IA, Vos S, Handels R, Visser PJ, (2010) Biomarkers as predictors for conversion from mild cognitive impairment to Alzheimer-type dementia: implications for trial design. J Alzheimers Dis 20: 881-891.
99. Matthews FE, Stephan BC, Bond J, McKeith I, Brayne C, (2007) Operationalization of mild cognitive impairment: a graphical approach. PLoS Med 4: 1615-1619.
100. Reitz C, Tang MX, Miller J, Green R, Luchsinger JA, (2009) Plasma homocysteine and risk of mild cognitive impairment. Dement Geriatr Cogn Disord 27: 11-17.
101. de Jager CA, Oulhaj A, Jacoby R, Refsum H, Smith AD, (2011) Cognitive and clinical outcomes of homocysteine-lowering B-vitamin treatment in mild cognitive impairment: a randomized controlled trial. Int J Geriatr Psychiatry 27: 592-600.